Vector-borne helminths of dogs and humans in Europe

Particle and Fibre Toxicology

Gioia Capelli⁵  Claudio Genchi¹  Dusan Petrić⁶  Donato Traversa²  Emanuele Brianti⁷  Filipe Dantas-Torres³  Domenico Otranto⁴ 

[1] Dipartimento di Patologia Animale, Igiene e Sanità Pubblica Veterinaria, Università degli Studi di Milan, Milan, Italy;Dipartimento di Scienze Biomediche Comparate, Università degli Studi di Teramo, Teramo, Italy;Departamento de Imunologia, Centro de Pesquisas Aggeu Magalhães (Fiocruz-PE), Recife, Pernambuco, Brazil;Dipartimento di Medicina Veterinaria, Università degli Studi di Bari, Bari, Valenzano, Italy;Istituto Zooprofilattico Sperimentale delle Venezie, Legnaro, Padova, Italy;Laboratory for Medical and Veterinary Entomology, Faculty of Agriculture, University of Novi Sad, Novi Sad, Serbia;Dipartimento di Sanità Pubblica Veterinaria, Università degli Studi di Messina, Messina, Italy

关键词: Control;    Treatment;    Vector;    Tick;    Mosquito;    Risk;    Europe;    Thelazia callipaeda;    Cercopithifilaria;    Onchocerca lupi;    Dirofilaria repens;    Dirofilaria immitis;    Zoonosis;   

Others  :  1228088
DOI  :  10.1186/1756-3305-6-16

 received in 2012-10-22, accepted in 2013-01-01,  发布年份 2013

【 摘 要 】

Presently, 45% of the total human population of Europe, as well as their domestic and companion animals, are exposed to the risk of vector-borne helminths (VBH) causing diseases. A plethora of intrinsic biological and extrinsic factors affect the relationship among helminths, vectors and animal hosts, in a constantly changing environment. Although canine dirofilarioses by Dirofilaria immitis and Dirofilaria repens are key examples of the success of VBH spreading into non-endemic areas, another example is represented by Thelazia callipaeda eyeworm, an emergent pathogen of dogs, cats and humans in several regions of Europe. The recent finding of Onchocerca lupi causing canine and human infestation in Europe and overseas renders the picture of VBH even more complicated. Similarly, tick-transmitted filarioids of the genus Cercopithifilaria infesting the skin of dogs were recently shown to be widespread in Europe. Although for most of the VBH above there is an increasing accumulation of research data on their distribution at national level, the overall impact of the diseases they cause in dogs and humans is not fully recognised in many aspects. This review investigates the reasons underlying the increasing trend in distribution of VBH in Europe and discusses the diagnostic and control strategies currently available. In addition, this article provides the authors’ opinion on some topics related to VBH that would deserve further scientific investigation.

【 授权许可】

   
2013 Otranto et al; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Otranto D, Eberhard ML: Zoonotic helminths affecting the human eye. Parasit Vectors 2011, 23:41.
• [2]Genchi C, Kramer LH, Rivasi F: Dirofilarial infections in Europe. Vector Borne Zoonotic Dis 2011, 11:1307-1317.
• [3]Morchón R, Carretón E, González-Miguel J, Mellado-Hernández I: Heartworm disease (Dirofilaria immitis) and their vectors in Europe - new distribution trends. Front Physiol 2012, 3:196.
• [4]Petrić D, Zgomba M, Bellini R, Becker N: Surveillance of Mosquito Populations: A Key Element to Understanding the Spread of Invasive Vector Species and Vector-Borne Diseases in Europe. In Essays on Fundamental and Applied Environmental Topics. Edited by Mihailović D. Hauppauge, New York: Nova Science Publishers; 2012:192-224.
• [5]Colwell DD, Dantas-Torres F, Otranto D: Vector-borne parasitic zoonoses: emerging scenarios and new perspectives. Vet Parasitol 2010, 24:14-21.
• [6]Otranto D, Brianti E, Latrofa MS, Annoscia G, Weigl S, Lia RP, Gaglio G, Napoli E, Giannetto S, Papadopoulos E, Mirò G, Dantas-Torres F, Bain O: On a Cercopithifilaria sp. transmitted by Rhipicephalus sanguineus: a neglected, but widespread filarioid of dogs. Parasit Vectors 2012, 5:1. BioMed Central Full Text
• [7]Genchi C, Rinaldi L, Mortarino M, Genchi M, Cringoli G: Climate and Dirofilaria infection in Europe. Vet Parasitol 2009, 163:286-292.
• [8]Becker N, Petrić D, Zgomba M, Boase C, Madon M, Dahl C, Kaiser A: Mosquitoes and their control. Berlin Heidelberg: Springer – Verlag; 2010.
• [9]Brianti E, Gaglio G, Napoli E, Giannetto S, Dantas-Torres F, Bain O, Otranto D: New insights into the ecology and biology of Acanthocheilonema reconditum (Grassi, 1889) causing canine subcutaneous filariosis. Parasitology 2012, 139(4):530-536.
• [10]Otranto D, Dantas-Torres F, Mallia E, DiGeronimo PM, Brianti E, Testini G, Traversa D, Lia RP: Thelazia callipaeda (Spirurida, Thelaziidae) in wild animals: report of new host species and ecological implications. Vet Parasitol 2009, 166:262-267.
• [11]Dorchies P, Chaudieu G, Simeon LA, Cazalot G, Cantacessi C, Otranto D: First reports of autochthonous eyeworm infection by Thelazia callipaeda (Spirurida, Thelaziidae) in dogs and cat from France. Vet Parasitol 2007, 149:294-297.
• [12]Ruytoor P, Dean E, Pennant O, Dorchies P, Chermette R, Otranto D, Guillot J: Ocular thelaziosis in dogs. France. Emerg Infect Dis 2010, 16:1943-1945.
• [13]Malacrida F, Hegglin D, Bacciarini L, Otranto D, Nägeli F, Nägeli C, Bernasconi C, Scheu U, Balli A, Marenco M, Togni L, Deplazes P, Schnyder M: Emergence of canine ocular thelaziosis caused by Thelazia callipaeda in southern Switzerland. Vet Parasitol 2008, 157:321-327.
• [14]Miró G, Montoya A, Hernández L, Dado D, Vázquez MV, Benito M, Villagrasa M, Brianti E, Otranto D: Thelazia callipaeda infection in dogs: a new parasite for Spain. Parasit Vectors 2011, 27:148.
• [15]Vieira L, Rodrigues FT, Costa A, Diz-Lopes D, Machado J, Coutinho T, Tuna J, Latrofa MS, Cardoso L, Otranto D: First report of canine ocular thelaziosis by Thelazia callipaeda in Portugal. Parasit Vectors 2012, 21:124.
• [16]Otranto D, Ferroglio E, Lia RP, Traversa D, Rossi L: Current status and epidemiological observation of Thelazia callipaeda (Spirurida, Thelaziidae) in dogs, cats and foxes in Italy: a "coincidence" or a parasitic disease of the Old Continent? Vet Parasitol 2003, 116:315-325.
• [17]Anderson RC: Nematode parasites of vertebrates. Their development and transmission. Wallingford, UK: CABI Publishing; 2000.
• [18]Otranto D, Lia RP, Cantacessi C, Testini G, Troccoli A, Shen JL, Wang ZX: Nematode biology and larval development of Thelazia callipaeda (Spirurida, Thelaziidae) in the drosophilid intermediate host in Europe and China. Parasitology 2005, 131:847-855.
• [19]Otranto D, Cantacessi C, Testini G, Lia RP: Phortica variegata as an intermediate host of Thelazia callipaeda under natural conditions: evidence for pathogen transmission by a male arthropod vector. Int J Parasitol 2006, 36:1167-1173.
• [20]Otranto D, Dutto M: Human thelaziosis Europe. Emerg Infect Dis 2008, 14:647-649.
• [21]Fuentes I, Montes I, Saugar JM, Latrofa S, Gárate T, Otranto D: Thelaziosis, a Zoonotic Infection, Spain, 2011. Emerg Infect Disin press
• [22]Egyed Z, Sréter T, Széll Z, Beszteri B, Oravecz , Márialigeti K, Varga I: Morphologic and genetic characterization of Onchocerca lupi infesting dogs. Vet Parasitol 2001, 102:309-319.
• [23]Széll Z, Erdélyi I, Sréter T, Albert M, Varga I: Canine ocular onchocercosis in Hungary. Vet Parasitol 2001, 97:245-251.
• [24]Komnenou A, Eberhard ML, Kaldrymidou E, Tsalie E, Dessiris A: Subconjunctival filariasis due to Onchocerca sp. in dogs: report of 23 cases in Greece. Vet Ophthalmol 2002, 5:119-126.
• [25]Hermosilla A, Hetzel U, Bausch M, Grübl J, Bauer C: First autochthonous case of canine ocular onchocercosis in Germany. Vet Rec 2005, 154:450-452.
• [26]Sréter-Lancz Z, Széll Z, Sréter T: Molecular genetic comparison of Onchocerca sp. infecting dogs in Europe with other spirurid nematodes including Onchocerca lienalis. Vet Parasitol 2007, 148:365-370.
• [27]Faísca P, Morales-Hojas R, Alves M, Gomes J, Botelho M, Melo M, Xufre A: A case of canine ocular onchocercosis in Portugal. Vet Ophthalmol 2010, 13:117-121.
• [28]Orihel TC, Ash LR, Holshuh HJ, Santenelli S: Onchocerciasis in a California dog. Am J Trop Med Hyg 1991, 44:513-517.
• [29]Eberhard ML, Ortega Y, Dial S, Schiller CA, Sears AW, Greiner E: Ocular Onchocerca infections in western United States. Vet Parasitol 2000, 90:333-338.
• [30]Zarfoss MK, Dubielzig RR, Eberhard ML, Schmidt KS: Canine ocular onchocerciasis in the United States: two new cases and a review of the literature. Vet Ophthalmol 2005, 8:51-57.
• [31]Labelle AL, Daniels JB, Dix M, Labelle P: Onchocerca lupi causing ocular disease in two cats. Vet Ophthalmol 2011, Suppl 1:105-110.
• [32]Sréter T, Széll Z: Onchocercosis: a newly recognized disease in dogs. Vet Parasitol 2008, 151:1-13.
• [33]Otranto D, Dantas-Torres F, Papadopoulos E, Petrić D, Ćupina AI, Bain O: Tracking the vector of Onchocerca lupi in a rural area of Greece. Emerg Infect Dis 2012, 18:1196-1200.
• [34]Bain O, Uni S, Takaoka H: A synthetic look at a twenty years old taxon, Cercopithifilaria its probable evolution. In Proceedings of the 10th International Congress of Parasitology (ICOPA):. Vancouver; 2002.
• [35]Otranto D, Brianti E, Dantas-Torres F, Weigl S, Latrofa MS, Gaglio G, Cauquil L, Giannetto S, Bain O: Morphological and molecular data on a Cercopithifilaria species from the dog skin. Vet Parasitol 2011, 182:221-229.
• [36]Otranto D, Brianti E, Dantas-Torres F, Miró G, Latrofa MS, Mutafchiev Y, Bain O: Species diversity of dermal microfilariae of the genus Cercopithifilaria infesting dogs in the Mediterranean region. Parasitology 2012, 23:1-10.
• [37]Brianti E, Otranto D, Dantas-Torres F, Weigl S, Latrofa MS, Gaglio G, Napoli E, Brucato G, Cauquil L, Giannetto S, Bain O: Rhipicephalus sanguineus (Ixodida, Ixodidae) as intermediate host of a canine neglected filarial species with dermal microfilariae. Vet Parasitol 2011, 183:330-337.
• [38]Otranto D, Brianti E, Abramo F, Gaglio G, Napoli E, Latrofa MS, Ramos RA, Dantas-Torres F, Bain O: Cutaneous distribution and localization of Cercopithifilaria sp. microfilariae in dogs. Vet Parasitol 2012, 190:143-150.
• [39]Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA: Fingerprints of global warming on wild animals and plants. Nature 2003, 421:57-60.
• [40]Khasnis AA, Nettleman MD: Global warming and infectious disease. Arch Med Res 2005, 36:689-696.
• [41]Purse BV, Mellor PS, Rogers DJ, Samuel AR, Mertens PP, Baylis M: Climate change and the recent emergence of bluetongue in Europe. Nat Rev Microbiol 2005, 3:171-181.
• [42]Semenza JC, Menne B: Climate change and infectious diseases in Europe. Lancet Infect Dis 2009, 9:365-375.
• [43]European Centre for Disease Prevention and Control (ECDC): First meeting of ECDC Expert Group on Climate Change. Stockholm; 2009. [http://www.ecdc.europa.eu/en/publications/Publications/0910_MER_First_Meeting_of_ECDC_Expert_Group_on_Climate_Change.pdf webcite]
• [44]Wilson N, Lush D, Baker MG: Meteorological and climate change themes at the 2010 International Conference on Emerging Infectious Diseases. Euro Surveill 2010, 15:pii=19627.
• [45]Sabatini A, Raineri V, Trovato G, Coluzzi M: Aedes albopictus in Italia e possibile diffusione della specie nell’area del mediterraneo. Parassitologia 1990, 32:301-304.
• [46]Cancrini G, Ricci I, Tessarin C, Gabrielli S, Pietrobelli M: Aedes albopictus is a natural vector of Dirofilaria immitis in Italy. Vet Parasitol 2003, 118:195-202.
• [47]Otranto D, Capelli G, Genchi C: Changing distribution patterns of canince vector borne disease in Italy: leishmaniosis vs. dirofilariosis. Parasit Vectors 2009, 26:Suppl 1 S2.
• [48]Genchi C, Rinaldi L, Cascone C, Mortasino M, Cringoli G: Is heartworm disease really spreading in Europe? Vet Parasitol 2005, 133:137-148.
• [49]Svobodova V, Misonova P: The potential risk of Dirofilaria immitis becoming established in the Czech Republic by imported dogs. Vet Parasitol 2005, 128:137-140.
• [50]Svobodova Z, Svobodova V, Genchi C, Forejtek P: The first report of autochthonous dirofilariosis in dogs in the Czech Republic. Helminthol 2006, 43:242-245.
• [51]Babal P, Kobzova D, Novak I, Dubinsky P, Jalili N: First case of cutaneous human dirofilariosis in Slovak Republic. Bratisl Lek List 2008, 109:486-488.
• [52]Tasić A, Rossi L, Tasić S, Miladinović-Tasić N, Ilić T, Dimitrijević S: Survey of canine dirofilariasis in Vojvodina. Serbia. Parasitol Res 2008, 103:1297-1302.
• [53]Otranto D, Dantas-Torres F: Canine and feline vector-borne diseases in Italy: current situation and perspectives. Parasit Vectors 2010, 3:2. BioMed Central Full Text
• [54]Ignjatovic Cupina A, Petric D, Papadopoulos E, Ptochos S, Otranto D, Dantas-Torres F, Mutafchiev J, Bain O: Notes on blackfly fauna in Western Thrace (northeastern Greece). Тhe British Simuliid Group Bulletinin press
• [55]Crosskey RW: The Natural History of Blackflies. British Museum (Natural History). John Wiley & Sons Ltd; 1990.
• [56]O’Dwyer LA, Burton DL: Potential meets reality: GIS and public health research in Australia. Aust N Z J Publ Heal 1998, 22:819-223.
• [57]Liebhold AM, Rossi RE, Kemp WP: Geostatistics and geographic information systems in applied insect ecology. Annu Rev Entomol 1993, 38:303-327.
• [58]Kitron U: Landscape ecology and epidemiology of vector-borne diseases: tools for spatial analysis. J Med Entomol 1998, 35:435-445.
• [59]Caminade C, Medlock JM, Ducheyne E, McIntyre KM, Leach S, Baylis M, Morse AP: Suitability of European climate for the Aedes albopictus: recent trends and future scenarios. J R Soc Interface 2012, 9:2708-2717.
• [60]Santa-Ana M, Khadem M, Capela R: Natural infection of Culex theileri (Diptera, Culicidae) with Dirofilaria immitis (Nematoda, Filarioidea) on Madeira Island, Portugal. J Med Entomol 2006, 43:104-106.
• [61]Cancrini G, Magi M, Gabrielli S, Arispici M, Tolari F, Dell'Omodarme M, Prati MC: Natural vectors of dirofilariasis in rural and urban areas of the Tuscan region, central Italy. J Med Entomol 2006, 43:574-579.
• [62]Petruschke G, Rossi L, Genchi C, Pollono F: Canine dirofilariasis in the canton of Ticino and in the neighboring areas of northern Italy. Schweiz Arch Tierheilkd 2001, 143:141-147.
• [63]Yildirim A, Inci A, Duzlu O, Biskin Z, Ica A, Sahin I: Aedes vexans and Culex pipiens as the potential vectors of Dirofilaria immitis in Central Turkey. Vet Parasitol 2011, 178:143-147.
• [64]Latrofa MS, Montarsi F, Ciocchetta S, Annoscia G, Dantas-Torres F, Ravagnan S, Capelli G, Otranto D: Molecular xenomonitoring of Dirofilaria immitis and Dirofilaria repens in mosquitoes from north-eastern Italy by real-time PCR coupled with melting curve analysis. Parasit Vectors 2012, 5:76. BioMed Central Full Text
• [65]Roggero C, Schaffner F, Bächli G, Mathis A, Schnyder M: Survey of Phortica drosophilid flies within and outside of a recently identified transmission area of the eye worm Thelazia callipaeda in Switzerland. Vet Parasitol 2010, 171:58-67.
• [66]McCall JW, Genchi C, Kramer LH, Guerrero J, Venco L: Heartworm disease in animals and humans. Adv Parasitol 2008, 66:193-285.
• [67]Pietrobelli M, Cancrini G, Capelli G, Frangipane di Regalbono A: Potential vectors for canine and humans dirofilariosis in North East Italy. Parassitologia 2000, 42(Suppl. 1):104.
• [68]Genchi C, Di Sacco B, Cancrini G: Epizootiology of canine and feline heartworm infection in northern Italy: possible mosquito vectors. Proceedings of heartworm Symposium 1992.
• [69]Labarthe N, Serrão ML, Melo YF, de Oliveira SJ, Lourenço-de-Oliveira R: Mosquito frequency and feeding habits in an enzootic canine dirofilariasis area in Niterói, state of Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 1998, 93:145-154.
• [70]Venco L, Genchi C, Genchi M, Grandi G, Kramer LH: Clinical evolution and radiographic findings of feline heartworm infection in asymptomatic cats. Vet Parasitol 2008, 158:232-237.
• [71]Ledesma N, Harrington L: Mosquito vectors of dog heartworm in the United States: vector status and factors influencing transmission efficiency. Top Companion Anim Med 2011, 26:178-185.
• [72]ECDC: European Network for Arthropod Vector Surveillance for Human Public Health. [http://ecdc.europa.eu/en/activities/diseaseprogrammes/emerging_and_vector_borne_diseases/Pages/VBORNET_maps.aspx webcite]
• [73]Cancrini G, Scaramozzino P, Gabrielli S, Di Paolo M, Toma L, Romi R: Aedes albopictus and Culex pipiens implicated as natural vectors of Dirofilaria repens in central Italy. J Med Entomol 2007, 44:1064-1066.
• [74]Cancrini G, Romi R, Gabrielli S, Toma L, Di Paolo M, Scaramozzino P: First finding of Dirofilaria repens in a natural population of Aedes albopictus. Med Vet Entomol 2003, 17:448-451.
• [75]Versteirt V, De Clercq E, Dekoninck W, Damiens D, Ayrinhac A, Jacobs F, Van Bortel W: Mosquito vectors of disease: spatial biodiversity, drivers of change, and risk". Final Report. Brussels: Belgian Science Policy; 2009:152. (Research Programme Science for a Sustainable Development); available online at http://www.belspo.be/belspo/SSD/science/Reports/FinalReport_MODIRISK%20ML.pdf webcite
• [76]Capelli G, Drago A, Martini S, Montarsi F, Soppelsa M, Delai N, Ravagnan S, Mazzon L, Schaffner F, Mathis A, Di Luca M, Romi R, Russo F: First report in Italy of the exotic mosquito species Aedes (Finlaya) koreicus, a potential vector of arboviruses and filariae. Parasit Vectors 2011, 28:188.
• [77]ECDC: European Network for Arthropod Vector Surveillance for Human Public Health. [http://ecdc.europa.eu/en/activities/diseaseprogrammes/emerging_and_vector_borne_diseases/Pages/VBORNET_maps.aspx webcite]
• [78]Di Cesare A, Castagna G, Meloni S, Milillo P, Latrofa S, Otranto D, Traversa D: Canine and feline infections by cardiopulmonary nematodes in central and southern Italy. Parasitol Res 2011, 109:S87-S96.
• [79]Gortazar C, Castillo JA, Lucientes J, Blanco JC, Arriolabengoa A, Calvete C: Factors affecting Dirofilaria immitis prevalence in red foxes in northeastern Spain. J Wildl Dis 1994, 30:545-547.
• [80]Magi M, Calderini P, Gabrielli S, Dell'Omodarme M, Macchioni F, Prati MC, Cancrini G: Vulpes vulpes: a possible wild reservoir for zoonotic filariae. Vector Borne Zoonotic Dis 2008, 8:249-252.
• [81]Shimalov VV, Pen'kevich VA: Helminth fauna of the wolf (Canis lupus Linnaeus, 1758) in Belorussian Polesie. Parazitologiia 2012, 46:118-126.
• [82]Kirkova Z, Ivanov A, Georgieva D: Dirofilariosis in dogs and wild carnivores in Bulgaria. In Dirofilaria immitis and D. repens in Dog and Cat and Human Infections Edited by Genchi C, Rinaldi L, Cringoli G. 2007.
• [83]Torres J, Feliu C, Fernández-Morán J, Ruíz-Olmo J, Rosoux R, Santos-Reis M, Miquel J, Fons R: Helminth parasites of the Eurasian otter Lutra lutra in southwest Europe. J Helminthol 2004, 78:353-359.
• [84]Molnar V, Pazár P, Rigó D, Máthé D, Fok E, Glávits R, Vajdovich P, Jacsó O, Balogh L, Sós E: Autochthonous Dirofilaria immitis infection in a ferret with aberrant larval migration in Europe. J Small Anim Pract 2010, 51:393-396.
• [85]Otranto D, Testini G, Deluca F, Hu M, Shamsi S, Gasser RB: Analysis of genetic variability within Thelazia callipaeda (Nematoda: Thelazioidea) from Europe and Asia by sequencing and mutation scanning of mitochondrial cytochrome c oxidase subunit 1. Mol Cell Probes 2005, 19:306-313.
• [86]Hermosilla C, Herrmann B, Bauer C: First case of Thelazia callipaeda infection in a dog in Germany. Vet Rec 2004, 154:568-669.
• [87]Pampiglione S, Canestri Trotti G, Rivasi F: Human dirofilariasis due to Dirofilaria (Nochtiella) repens in Italy: a review of word literature. Parassitologia 1995, 37:149-193.
• [88]Pampiglione S, Rivasi F, Gustinelli A: Dirofilarial human cases in the old world, attributed to Dirofilaria immitis: a critical analysis. Histopathology 2009, 54:192-204.
• [89]Miliaras D, Meditskou S, Kelekis A, Papachristos I: Human pulmonary Dirofilariasis: one more case in Greece suggests that Dirofilaria is a rather common cause of coin lesions in the lungs in endemic areas of Europe. Int J Immunopathol Pharmacol 2010, 23:345-348.
• [90]Morchón R, Moya I, González-Miguel J, Montoya MN, Simón F: Zoonotic Dirofilaria immitis infections in a province of Northern Spain. Epidemiol Infect 2010, 138(3):380-383.
• [91]Avellis FO, Kramer LH, Mora P, Bartolino A, Benedetti P, Rivasi F: A case of human conjunctival dirofilariosis by Dirofilaria immitis in Italy. Vector Borne Zoonotic Dis 2011, 11:451-452.
• [92]Otranto D, Sakru N, Testini G, Gürlü VP, Yakar K, Lia RP, Dantas-Torres F, Bain O: Case report: first evidence of human zoonotic infection by Onchocerca lupi (Spirurida, Onchocercidae). Am J Trop Med Hyg 2011, 84:55-58.
• [93]Otranto D, Dantas-Torres F, Cebeci Z, Yeniad B, Buyukbabani N, Boral OB, Gustinelli A, Mounir T, Mutafchiev Y, Bain O: Human ocular filariasis: further evidence on the zoonotic role of Onchocerca lupi. Parasit Vectors 2012, 27:84.
• [94]Shen J, Gasser RB, Chu D, Wang Z, Yuan X, Cantacessi C, Otranto D: Human thelaziosis-a neglected parasitic disease of the eye. J Parasitol 2006, 92:872-875.
• [95]Genchi C, Rossi L, Cardini G, Kramer LH, Venco L, Casiraghi M, Genchi M, Agostini A: Full season efficacy of moxidectin microsphere sustained release formulation for prevention of hearworm (Dirofilaria immitis) infection in dogs. Vet Parasitol 2002, 110:85-91.
• [96]Genchi M, Pengo G, Genchi C: Efficacy of moxidectin microsphere sustained release formulation for the prevention of subcutaneous filarial infections (Dirofilaria repens) in dogs. Vet Parasitol 2010, 170:167-69.
• [97]Knight DH, Lok JB: Seasonal timing of heartworm chemoprophylaxis in the United States. In Proceedings of the Heartworm Symposium 1995. Washington, D.C., U.S.A: American Hearthworm Society; 1995:36-42.
• [98]Slocombe JOB, Bhactendu-Srivastava B, Surgeoner GA: The transmission period for heartworm in Canada. In Proceedings of the Heartworm Symposium 1995. Washington, D.C., U.S.A: American Hearthworm Society; 1995:43-48.
• [99]Bowman DD: Georgi's Parasitology for Veterinarians. 7th edition. Philadelphia: Saunders Elsevier; 2002.
• [100]Romi R, Severini F, Toma L: Cold acclimation and overwintering of female Aedes albopictus in Roma. J Am Mosq Control Assoc 2006, 22:149-151.
• [101]Nelson CT, McCall JW, Rubin SB, Buzhardt LF, Doiron DW, Graham W, Longhofer SL, Guerrero J, Robertson-Plough C, Paul A: Guidelines for the diagnosis, prevention and management of heartworm (Dirofilaria immitis) infection in dogs. Vet Parasitol 2005, 133:255-266.
• [102]McCall JW, Guerrero J, Roberts RE, Supakorndej N, Mansour AE, Dzimianski MT, McCall SD: Further evidence of clinical prophylactic (reach-back) and adulticidal activity of monthly administration of ivermectin and pyrantel pamoate (Heartgard Plus) in dogs experimentally infected with heartworms. In Proceedings of the American Heartworm Symposium. Edited by Seward L. Batavia, IL; 2001:189-200.
• [103]Rawlings CA, Bowman DD, Howerth EW, Stansfield DG, Legg W, Luempert LG: Response of dogs treated with ivermectin or milbemycin starting at various intervals after Dirofilaria immitis infection. Vet Ther 2001, 2:193-207.
• [104]Venco L, McCall JW, Guerrero J, Genchi C: Efficacy of long-term monthly administration of ivermectin on the progress of naturally acquired heartworm infection in dogs. Vet Parasitol 2004, 124:259-268.
• [105]Atkins C, Miller MW: Is there a better way to administer heartworm adulticidal therapy? Vet Med 2003, 98:310-317.
• [106]Kramer L, Grandi G, Leoni M, Passeri B, McCall J, Genchi C, Mortarino M, Bazzocchi C: Wolbachia and its influence on the pathology and immunology of Dirofilaria immitis infection. Vet Parasitol 2008, 158:191-195.
• [107]Bazzocchi C, Mortarino M, Grandi G, Kramer LH, Genchi C, Bandi C, Genchi M, Sacchi L, McCall JW: Combined ivermectin and doxycycline treatment has microfilaricidal and adulticidal activity against Dirofilaria immitis in experimentally infected dogs. Int J Parasitol 2008, 38:1401-1410.
• [108]Grandi G, Quintavalla C, Mavropoulou A, Genchi M, Gnudi G, Bertoni G, Kramer LH: A combination of doxycycline and ivermectin is adulticidal in dogs with naturally acquired heartworm disease (Dirofilaria immitis). Vet Parasitol 2010, 169:347-351.
• [109]Baneth G, Volansky Z, Anug Y: Dirofilaria repens infection in a dog: diagnosis and treatment with melarsomine and doramectin. Vet Parasitol 2002, 105:173-178.
• [110]Fok E, Jacsó O, Szebeni Z, Gyorffy A, Sükösd L, Lukács Z, Schaper R: Elimination of Dirofilaria (syn. Nochtiella) repens microfilariae in dogs with monthly treatments of moxidectin 2.5%/imidacloprid 10% (Advocate, Bayer) spot-on. Parasitol Res 2010, 106:1141-1149.
• [111]Jacsó O, Fok E, Kiss G, Kökény G, Lang Z: Preliminary findings on the efficacy of selamectin in the treatment of dogs naturally infected with Dirofilaria repens. Acta Vet Hung 2010, 58:405-412.
• [112]Traversa D, Aste G, Milillo P, Capelli G, Pampurini F, Tunesi C, Santori D, Paoletti B, Boari A: Autochthonous foci of canine and feline infections by Dirofilaria immitis and Dirofilaria repens in central Italy. Vet Parasitol 2010, 169:128-132.
• [113]Traversa D, Aste G, Di Cesare A, Paoletti B, Di Tommaso M, Di Giulio E, Pampurini F, Tunesi C, Boari A: Efficacy of a single administration of a spot-on solution containing imidacloprid 10%/moxidectin 2.5% in eliminating Dirofilaria repens microfilariae in naturally infected dogs. Vet Parasitol 2011, 179:107-112.
• [114]Hellmann K, Heine J, Braun G, Paran-Dobesova R, Svobodova V: Evaluation of the therapeutic and preventive efficacy of 2.5% moxidectin / 10% imidacloprid (Advocate(®), Bayer animal health) in dogs naturally infected or at risk of natural infection by Dirofilaria repens. Parasitol Res 2011, 109:S77-86.
• [115]Arita N, Yamane I, Takemura N: Comparison of canine heartworm removal rates using flexible alligator forceps guided by transesophageal echocardiography and fluoroscopy. J Vet Med Sci 2003, 65:259-261.
• [116]Lindemann BA, McCall JW: Microfilaricidal activity of ivermectin against Dipetalonema reconditum. J Vet Pharmacol Ther 1983, 6:75-76.
• [117]Venco L, Kramer L, Genchi C: Heartworm disease in dogs: unusual clinical cases. Vet Parasitol 2005, 133:207-218.
• [118]Rossi L, Peruccio C: Thelaziosi oculare nel Cane: aspetti clinici e terapeutici. Veterinaria 1989, B:47-50.
• [119]Lia RP, Traversa D, Agostini A, Otranto D: Field efficacy of moxidectin 1 per cent against Thelazia callipaeda in naturally infected dogs. Vet Rec 2004, 154:143-145.
• [120]Bianciardi P, Otranto D: Treatment of dog thelaziosis caused by Thelazia callipaeda (Spirurida, Thelaziidae) using a topical formulation of imidacloprid 10% and moxidectin 2.5%. Vet Parasitol 2005, 129:89-93.
• [121]Rossi L, Rigano C, Tomio E, Frassetto D, Ferroglio E: Use of sustained-release moxidectin to prevent eyeworm (Thelazia callipaeda) infection in dogs. Vet Rec 2007, 161:820-821.
• [122]Ferroglio E, Rossi L, Tomio E, Schenker R, Bianciardi P: Therapeutic and prophylactic efficacy of milbemycin oxime (Interceptor) against Thelazia callipaeda in naturally exposed dogs. Vet Parasitol 2008, 154:351-353.
• [123]Sloss MW, Kemp RL, Zajac AM: Veterinary Clinical Parasitology. Iowa, USA: University Press; 1994.
• [124]Taylor MA, Coop RL, Wall RL: Veterinary Parasitology. Oxford: Blackwell Publishing; 2007.
• [125]Venco L, Genchi M, Genchi C, Gatti D, Kramer L: Can heartworm prevalence in dogs be used as provisional data for assessing the prevalence of the infection in cats? Vet Parasitol 2011, 176:300-303.
• [126]Casiraghi M, Mazzocchi C, Mortarino M, Ottina E, Genchi C: A simple molecular method for discrimination common filarial nematodes of dogs (Canis familiaris). Vet Parasitol 2006, 141:368-372.
• [127]Rishniw M, Barr SC, Simpson KW, Frongillo MF, Franz M, Dominguez Alpizar JL: Discrimination between six species of canine microfilariae by a single polymerase chain reaction. Vet Parasitol 2006, 135:303-314.
• [128]Oh HW, Jun HK, You MJ, Hayasaki M, Song KH: Ectopic migration of an adult heartworm in a dog with dirofilariasis (case report). Korean J Parasitol 2008, 46:171-173.
• [129]Megat Abd Rani PA, Irwin PJ, Gatne M, Coleman GT, McInnes LM, Traub RJ: A survey of canine filarial diseases of veterinary and public health significance in India. Parasit Vectors 2010, 3:30. BioMed Central Full Text
• [130]Latrofa MS, Dantas-Torres F, Annoscia G, Genchi M, Traversa D, Otranto D: A duplex real-time polymerase chain reaction assay for the detection of and differentiation between Dirofilaria immitis and Dirofilaria repens in dogs and mosquitoes. Vet Parasitol 2012, 185:181-185.
• [131]Latrofa MS, Weigl S, Dantas-Torres F, Annoscia G, Traversa D, Brianti E, Otranto D: A multiplex PCR for the simultaneous detection of species of filarioids infesting dogs. Acta Trop 2012, 122(1):150-154.